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Transcriptome-Wide Analysis of the Response of the Thecosome Pteropod Clio Pyramidata to Short-Term CO2 Exposure

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Transcriptome-Wide Analysis of the Response of the Thecosome Pteropod Clio Pyramidata to Short-Term CO2 Exposure See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/279754159 Transcriptome-wide analysis of the response of the thecosome pteropod Clio pyramidata to short-term CO2 exposure Article in Comparative Biochemistry and Physiology Part D Genomics and Proteomics · June 2015 DOI: 10.1016/j.cbd.2015.06.002 · Source: PubMed CITATIONS READS 5 44 3 authors, including: AE Maas Ann M Tarrant Bermuda Institute of Ocean Sciences Woods Hole Oceanographic Institution 16 PUBLICATIONS 133 CITATIONS 65 PUBLICATIONS 888 CITATIONS SEE PROFILE SEE PROFILE Available from: AE Maas Retrieved on: 02 August 2016 1 Transcriptome-wide analysis of the response of the thecosome pteropod Clio pyramidata to 2 short-term CO2 exposure 3 4 5 1,2* 1 1 6 Amy E. Maas , Gareth L. Lawson , and Ann M. Tarrant 7 8 1. Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA 9 2. Current address: Bermuda Institute of Ocean Sciences, St. George’s GE01, Bermuda 10 11 *Corresponding author e-mail: [email protected]. Maas et al. 1 12 Abstract 13 Thecosome pteropods, a group of calcifying holoplanktonic molluscs, have recently become a 14 research focus due to their potential sensitivity to increased levels of anthropogenic dissolved 15 CO2 in seawater and the accompanying ocean acidification. Some populations, however, already 16 experience high CO2 in their natural distribution during diel vertical migrations. To achieve a 17 better understanding of the mechanisms of pteropod calcification and physiological response to 18 this sort of short duration CO2 exposure, we characterized the gene complement of Clio 19 pyramidata, a cosmopolitan diel migratory thecosome, and investigated its transcriptomic 20 response to experimentally manipulated CO2 conditions. Individuals were sampled from the 21 Northwest Atlantic in the fall of 2011 and exposed to ambient conditions (~380 ppm) and 22 elevated CO2 (~800 ppm, similar to levels experienced during a diel vertical migration) for ~10 23 hrs. Following this exposure the respiration rate of the individuals was measured. We then 24 performed RNA-seq analysis, assembled the C. pyramidata transcriptome de novo, annotated the 25 genes, and assessed the differential gene expression patterns in response to exposure to elevated 26 CO2. Within the transcriptome, we identified homologs of genes with known roles in 27 biomineralization in other molluscs, including perlucin, calmodulin, dermatopontin, calponin, 28 and chitin synthases. Respiration rate was not affected by short-term exposure to CO2. Gene 29 expression varied greatly among individuals, and comparison between treatments indicated that 30 C. pyramidata down-regulated a small number of genes associated with aerobic metabolism and 31 up-regulated genes that may be associated with biomineralization, particularly collagens and C- 32 type lectins. These results provide initial insight into the effects of short term CO2 exposure on 33 these important planktonic open-ocean calcifiers, pairing respiration rate and the gene expression 34 level of response, and reveal candidate genes for future ecophysiological, biomaterial and 35 phylogenetic studies. 36 37 38 39 40 41 42 43 44 45 46 47 48 49 Keywords: acidification, climate change, gastropod, lectin, mollusc, RNA-seq, transcriptomics Maas et al. 2 50 Introduction 51 The dissolution of anthropogenic carbon dioxide (CO2) into seawater, or ocean acidification 52 (OA), stands to impact a broad variety of marine organisms, especially those that secrete calcium 53 carbonate (CaCO3) shells or skeletons (Fabry et al., 2008). As CO2 equilibrates into seawater, pH 54 and the concentration of carbonate ions decrease, causing CaCO3 to dissociate and affecting the 55 ability of calcifying animals to create and maintain calcareous structures (Gattuso et al., 1999; 56 Riebesell et al., 2000). Furthermore, decreasing pH in the water alters the acid-base balance of 57 the intra- and extracellular fluids of marine organisms (Miles et al., 2007; Seibel and Fabry, 58 2003; Seibel and Walsh, 2001). Since CO2 is produced naturally as a byproduct of respiration, all 59 organisms have physiological mechanisms for maintaining internal cellular pH. These 60 compensatory mechanisms may, however, cease to function if internal acidosis becomes too 61 severe over short time scales and generally fail over extended periods of internal pH imbalance. 62 Classical organismal-level metrics (e.g., metabolic rate, calcification, mortality) have revealed a 63 complex pattern of intra- and inter-specific variation in responses to CO2 exposure (reviewed in 64 Hendriks et al., 2010; Kroeker et al., 2013; Kroeker et al., 2010). The variability in these 65 responses, and their dependence on duration of exposure or co-varying stressors, suggest that 66 there is an energetic cost associated with compensating for high CO2 (e.g.,69 Cummings et al., 67 2011; Langenbuch and Pörtner, 2004; Stumpp et al., 2011b). 7068 71 One group thought to be particularly sensitive to OA is the thecosomatous (i.e., shelled) 72 pteropods. These holoplanktonic gastropods, related to terrestrial snails and also known as sea 73 butterflies, produce thin shells made of aragonite, a highly soluble form of CaCO3. In temperate 74 and polar seas, thecosomes can become a numerically dominant member of the zooplankton 75 community (Hunt et al., 2008). This causes them to be significant consumers of primary 76 production, serve as a key food item for commercially important fish, seabirds and whales, and 77 substantially contribute to carbon flux to the deep ocean (reviewed in: Bednaršek et al., 2012a; 78 Lalli and Gilmer, 1989; Manno et al., 2010). Studies of thecosome biomineralization have 79 revealed that increasing CO2 levels result in decreased calcification and shell degradation 80 (Bednaršek et al., 2014; Bednaršek et al., 2012b; Comeau et al., 2009; Lischka and Riebesell, 81 2012; Manno et al., 2012). It remains unclear whether the decreases in calcification documented 82 in thecosomes at high CO2 concentrations are a result of their inability to form carbonates, or 83 rather are a result of a re-allocation of energy, as has been described in other species (e.g., 84 Melzner et al., 2013; Stumpp et al., 2012). 85 86 87 The impact of CO2 on the metabolic rate and mortality of thecosome pteropods has been shown 88 to be variable, and highly dependent upon the presence of co-varying stressors such as salinity, 89 temperature and feeding history (Comeau et al., 2010a; Lischka and Riebesell, 2012; Maas et al., 90 in review; Manno et al., 2012; Seibel et al., 2012). In contrast to laboratory findings concerning 91 the effects of under-saturation on pteropods, Maas et al. (2012) found that some species of 92 thecosomes regularly experience conditions of high CO2 and aragonite saturation states <1 93 during diel vertical migrations into an oxygen minimum zone in the eastern tropical North Maas et al. 3 94 Pacific, and do not respond to short-term laboratory CO2 exposure with a change in metabolic 95 rate. This suggests that in some thecosome species there is a potential adaptation or acclimation 96 to high CO2, at least over short periods. Supporting this idea, more recent work comparing 97 thecosomes from the Northeast Pacific and Northwest Atlantic revealed that the metabolic rates 98 of multiple thecosome pteropod species are not affected by short-term exposure to CO2 at the 99 levels predicted for the coming century (800 ppm; Maas et al., in review). Exploring the 100 physiological mechanisms these species use to cope with short-term CO2 exposure may provide 101 insight into what duration and level of exposure to anthropogenic CO2 thecosomes can tolerate. 102 Elucidating these mechanisms will also provide a means to characterize the physiological 103 condition of pteropods within natural populations and enable development of molecular 104 biomarkers indicating responses to elevated CO2 exposure. 105 106 107 An increasing number of studies have employed molecular methods to disentangle the complex 108 picture associated with CO2 response, revealing changes in expression of genes with a known or 109 predicted role in acid-base balance, apoptosis, biomineralization, development, protein synthesis, 110 energetic metabolism, and stress responses (Hüning et al., 2013; Kaniewska et al., 2012; 111 Kurihara et al., 2012; Moya et al., 2012). For example, Moya et al. (2012) showed that coral 112 larvae respond to CO2 through changes in gene expression that were consistent with suppressed 113 metabolism and changes in calcification. They also discovered an unexpected lack of response in 114 ion transport proteins and a down-regulation of carbonic anhydrase genes. Relatively few studies 115 have matched observations of altered gene expression with organismal-level observations such 116 as developmental delays or changes in metabolic rate (e.g., Stumpp et al., 2011b). Many of the 117 previous studies have used quantitative PCR (qPCR), a targeted approach which involves 118 picking a small number of genes a priori such as studies with mussel (Hüning et al., 2013), 119 abalone (Zippay and Hofmann, 2010), urchin (Stumpp et al., 2011a), and oyster (Liu et al., 120 2012), or using microarrays, which have historically only been done with well-studied organisms 121 such as urchins (Evans et al., 2013; O'Donnell et al., 2010; Todgham and Hofmann, 2009) and 122 corals (Kaniewska et al., 2012). 123 124 125 Despite the benefits of using gene expression studies for understanding the response to CO2 at a 126 mechanistic level, there have been no published studies of pteropod gene expression to date. 127 High throughput RNA sequencing (RNA-seq) methods enable quantitative characterization of 128 gene expression patterns across the transcriptome (Ekblom and Galindo, 2011; Vijay et al., 129 2012). When a reference genome is not available, a transcriptome can be assembled de novo 130 from millions of short reads. The reads from individual samples can then be mapped onto this 131 reference transcriptome for a comprehensive assessment of differential gene expression.
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